Abstract
Genotype and phenotype in mobile organisms can be defined by various factors such as environmental, biological and geographical. Brown noddies Anous stolidus are pan-tropical seabirds breeding at different times, with migratory and resident populations in six islands throughout 20° of latitude in the Southwestern Atlantic Ocean. If environmental heterogeneity plays a key role in their population biology, we would expect significant genetic structure among colonies. However, absence of genetic structure between phenotypically different populations could play a scenario of ecological plasticity. To test these hypotheses, we used a model-based integrative approach combining genetic (mtDNA and ultraconserved elements) and morphological data of the brown noddy (n = 122) along with environmental variables and isotopic niches. We uncovered low levels of genetic structure, with 16 haplotypes for mtDNA and a signal of an ancient population expansion. Ultraconserved elements indicated that all colonies belong to the same genetic population (K = 1) and revealed substantial endogamy. However, phenotype differed both by biometric measures and isotopic niches between most pairs of populations. Although individuals from the northernmost colony are larger than the others, they are genetically similar, indicating a wide reaction norm for this species. Our results indicate the Southwestern Atlantic populations of the brown noddy are panmictic, but ecologically and morphologically diverse.
Similar content being viewed by others
Data availability
DNA sequences are available at GenBank under the accession numbers: PP176671-PP176781 and PP179903-PP179967 for mtDNA (ND2 and ATPase6/8, respectively). SNPs matrix from UCEs loci are available on Zenodo (https://doi.org/10.5281/zenodo.10524760). Stable isotope analysis results and biometric measures are provided as supplementary material.
References
Araujo MC, Cintra MM (2009) Modelagem matemática da circulação oceânica na região equatorial. In: Viana DL, Hazin FHV, de Souza MAC (eds) O arquipélago de São Pedro e São Paulo: 10 anos de estação científica. SECIRM, Brasilia, pp 7–113
Beerli P, Mashayekhi S, Sadeghi M, Khodaei M, Shaw K (2019) Population genetic inference with Migrate. Curr Protoc Bioinf 68:e87. https://doi.org/10.1002/cpbi.87
BirdLife International (2023) Species factsheet: Anous stolidus. Downloaded from https://www.birdlife.org
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170
Bosch S, Fernandez S (2022) sdmpredictors: species distribution modelling predictor datasets. R package version 0.2.12. See https://CRAN.R-project.org/package=sdmpredictors
Bouckaert R, Heled J, Kühnert D, Vaughan T, Wu C-H, Xie D, Suchard MA, Rambaut A, Drummond AJ (2014) BEAST 2: a software platform for bayesian evolutionary analysis. PLoS Comput Biol 10:e1003537. https://doi.org/10.1371/journal.pcbi.1003537
Branco JO (2004) Aves Marinhas e Insulares Brasileiras: Bioecologia e Conservação. Univali: Itajaí
Brown WY Jr, Robertson WY (1975) Longevity of the brown noddy. Bird-Band 46:250–251
Burchett WW, Ellis AR, Solomon WH, Bathke AC (2017) Nonparametric inference for multivariate data: the R package npmv. J Stat Softw 76:1–18. https://doi.org/10.18637/jss.v076.i04
Byerly PA, Chesser RT, Fleischer RC, McInerney N, Przelomska NA, Leberg PL (2023) Conservation genomics reveals low connectivity among populations of threatened roseate terns (Sterna dougallii) in the Atlantic Basin. Conserv Genet 24:331–345. https://doi.org/10.1007/s10592-023-01505-6
Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL (2009) BLAST+: architecture and applications. BMC Bioinformatics 10:421. https://doi.org/10.1186/1471-2105-10-421
Campolina C, Gomes HB, Rodrigues M, Barbosa B (2002) Instabilidade da colônia reprodutiva de Anous stolidus (Aves: Laridae) no Arquipélago Dos Abrolhos, Bahia. Caderno de Resumos do. XXIV Congresso Brasileiro de Zoologia, Itajaí
Carrea C, Burridge CP, Wienecke B, Emmerson LM, White D, Miller KJ (2019) High vagility facilitates population persistence and expansion prior to the last glacial maximum in an Antarctic top predator: the snow petrel (Pagodroma nivea). J Biogeogr 46:442–453. https://doi.org/10.1111/jbi.13513
Chardine JW, Morris RD, Gochfeld M, Burger J, Kirwan GM, Garcia EFJ (2020) Brown noddy (Anous stolidus), version 1.0. In birds of the world (eds Billerman SM). Cornell Lab of Ornithology, Ithaca
Clapp RB, Klimkiewicz MK, Kennard JH (1982) Longevity records of North American birds: Gaviidae through Alcidae. J Field Ornithol 53:81–208
CLIMAP Project Members (1976) The surface of the ice-age earth. Science 191:1131–1137
Coulson JC (2001) Colonial breeding in seabirds. Biology of Marine Birds (eds Schreiber EA, Burger J). CRC, Boca Raton, pp 87–114
Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, Handsaker R, Lunter G, Marth G, Sherry ST, McVean G, Durbin R, 1000 Genomes Project Analysis Group (2011) The variant call Format and VCFtools. Bionformatics 27:2156–2158. https://doi.org/10.1093/bioinformatics/btr330
Danecek P, Bonfield JK, Liddle J, Marshall J, Ohan V, Pollard MO, Whitwham A, Keane T, McCarthy SA, Davies RM, Li H (2021) Twelve years of SAMtools and BCFtools. GigaScience 10:1–4. https://doi.org/10.1093/gigascience/giab008
Diniz-Filho JAF, Soares TN, Lima JS, Dobrovolski R, Landeiro VL, Telles MPC, Rangel TF, Bini LM (2013) Mantel test in population genetics. Genet Mol Biol 36:475–485. https://doi.org/10.1590/S1415-47572013000400002
Do C, Waples RS, Peel D, Macbeth GM, Tillett BJ, Ovenden JR (2014) NeEstimator V2: re-implementation of software for the estimation of contemporary effective population size (ne) from genetic data. Mol Ecol Resour 14:209–214. https://doi.org/10.1111/1755-0998.12157
Dorward DF, Ashmole NP (1963) Notes on the biology of the brown noddy Anous stolidus on Ascension Island. Ibis 103b:447–457. https://doi.org/10.1111/j.1474-919X.1963.tb06765.x
Drummond AJ, Rambaut A, Shapiro BETH, Pybus OG (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22:1185–1192. https://doi.org/10.1093/molbev/msi103
Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361. https://doi.org/10.1007/s12686-011-9548-7
Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x
Faircloth BC (2013) Illumiprocessor: a trimmomatic wrapper for parallel adapter and quality trimming. https://doi.org/10.6079/J9ILL
Faircloth BC (2015) PHYLUCE is a software package for the analysis of conserved genomic loci. Bioinformatics 32:786–788. https://doi.org/10.1093/bioinformatics/btv646
Faria PJ, Baus E, Morgante JS, Bruford MW (2007) Challenges and prospects of population genetic studies in terns (Charadriiformes, Aves). Genet Mol Biol 30:681–689. https://doi.org/10.1590/S1415-47572007000400029
Faria PJ, Campos FP, Branco JO, Musso CM, Morgante JS, Bruford MW (2010) Population structure in the South American tern Sterna hirundinacea in the South Atlantic: two populations with distinct breeding phenologies. J Avian Biol 41:378–387. https://doi.org/10.1111/j.1600-048X.2009.04902.x
Frichot E, Francois O (2015) LEA: an R package for Landscape and Ecological Association studies. Methods Ecol Evol 6:925–929. https://doi.org/10.1111/2041-210X.12382
Frichot E, Mathieu F, Trouillon T, Bouchard G, Francois O (2014) Fast and efficient estimation of individual ancestry coefficients. Genetics 194:973–983. https://doi.org/10.1534/genetics.113.160572
Friesen VL (2015) Speciation in seabirds: why are there so many species… and why aren’t there more? J Ornithol 156:27–39. https://doi.org/10.1007/s10336-015-1235-0
Fry B (2006) Stable Isotope Ecology. Springer, New York
Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 2:915–925. https://doi.org/10.1093/genetics/147.2.915
Garrett LJH, Myatt JP, Sadler JP, Dawson DA, Hipperson H, Colbourne JK, Dickey RC, Weber SB, Reynolds SJ (2020) Spatio-temporal processes drive fine-scale genetic structure in an otherwise panmictic seabird population. Sci Rep 10:20725. https://doi.org/10.1038/s41598-020-77517-w
Gómez-Díaz E, González-Solís J (2007) Geographic assignment of seabirds to their origin: combining morphologic, genetic, and biogeochemical analyses. Ecol Appl 17:1484–1498. https://doi.org/10.1890/06-1232.1
Goudet J, Jombart T (2022) hierfstat: Estimation and Tests of Hierarchical F-Statistics. R package version 0.5–11. See https://CRAN.R-project.org/package=hierfstat
Griffiths R, Daan S, Dijkstra C (1996) Sex identification in birds using two CHD genes. Proc Biol Sci 163:1251–1256. https://doi.org/10.1098/rspb.196.0184
Hamilton MB (2021) Population Genetics. Wiley, New Jersey
Harvey MG, Aleixo A, Ribas CC, Brumfield RT (2017) Habitat association predicts genetic diversity and population divergence in Amazonian birds. Am Nat 190:631–648. https://doi.org/10.1086/693856
Herman RW, Winder BM, Dittmann DL, Harvey MG (2022) Fine-scale population genetic structure and barriers to gene flow in a widespread seabird (Ardenna pacifica). Biol J Linn Soc 137:125–136. https://doi.org/10.1093/biolinnean/blac091
Hijmans RJ (2022) raster: Geographic Data Analysis and Modeling. R package version 3.5–15. See https://CRAN.R-project.org/package=raster
Ho SYW, Duchêne S (2014) Molecular-clock methods for estimating evolutionary rates and timescales. Mol Ecol Resour 23:5947–5965. https://doi.org/10.1111/mec.12953)
Huot Y, Babin M, Bruyant F, Grob C, Twardowski MS, Claustre H (2007) Relationship between photosynthetic parameters and different proxies of phytoplankton biomass in the subtropical ocean. Biogeosciences 4:853–868. https://doi.org/10.5194/bg-4-853-2007
Instituto Chico Mendes de Conservação da Biodiversidade (ICMBIO) (2020) Relatório anual do Programa de Monitoramento das Aves Marinhas do Parque Nacional Marinho dos Abrolhos (2019). Caravelas, Brasil
Jackson AL, Parnell AC, Inger R, Bearhop S (2011) Comparing isotopic niche widths among and within communities: SIBER - stable isotope bayesian ellipses in R. J Anim Ecol 80:595–602. https://doi.org/10.1111/j.1365-2656.2011.01806.x
Jombart T (2008) Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405. https://doi.org/10.1093/bioinformatics/btn129
Kellner K (2019) jagsUI: A Wrapper Around ‘rjags’ to Streamline ‘JAGS’ Analyses. R package version 1.5.1. See https://CRAN.R-project.org/package=jagsUI
Kinas PG, Andrade HA (2010) Introdução à Análise Bayesiana (com R). maisQ-nada, Porto Alegre
Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I (2015) Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour 15:1179–1191. https://doi.org/10.1111/1755-0998.12387
Lah L, Trense D, Benke H, Berggren P, Gunnlaugsson Þ, Lockyer C, Öztürk A, Öztürk B, Pawliczka AR, Siebert U, Skóra K, Víkingsson G, Tiedemann R (2016) Spatially explicit analysis of genome-wide SNPs detects subtle population structure in a mobile marine mammal, the harbor porpoise. PLoS ONE 11:e0162792. https://doi.org/10.1371/journal.pone.0162792
Larmuseau M, Raeymaekers J, Hellemans B, Van Houdt JKJ, Volckaert FAM (2010) Mito-nuclear discordance in the degree of population differentiation in a marine goby. Heredity 105:532–542. https://doi.org/10.1038/hdy.2010.9
Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25:1754–1760. https://doi.org/10.1093/bioinformatics/btp324
Lombal AJ, O’Dwyer JE, Friesen V, Woehler EJ, Burridge CP (2020) Identifying mechanisms of genetic differentiation among populations in vagile species: historical factors dominate genetic differentiation in seabirds. Biol Rev 95:625–651. https://doi.org/10.1111/brv.12580
Lynch M (2010) Evolution of the mutation rate. Trends Genet 26:345–352. https://doi.org/10.1016/j.tig.2010.05.003
Mancini PL, Hobson KA, Bugoni L (2014) Role of body size in shaping the trophic structure of tropical seabird communities. Mar Ecol Prog Ser 497:243–257. https://doi.org/10.3354/meps10589
Mancini PL, Serafini P, Bugoni L (2016) Breeding seabird populations in Brazilian oceanic islands: historical review, update and a call for census standardization. Rev Bras Ornitol 24:94–115. https://doi.org/10.1007/BF03544338
Mason NA, Olvera-Vital A, Lovette IJ, Navarro-Sigüenza AG (2018) Hidden endemism, deep polyphyly, and repeated dispersal across the Isthmus of Tehuantepec: diversification of the white-collared seedeater complex (Thraupidae: Sporophila torqueola) Ecol Evol 8:1867–1881. https://doi.org/10.1002/ece3.3799
Meirmans PG (2014) Nonconvergence in bayesian estimation of migration rates. Mol Ecol Resour 14:726–733. https://doi.org/10.1111/1755-0998.12216
Meredith M, Kruschke J (2020) HDInterval: Highest (Posterior) Density Intervals. R package version 0.2.2. See https://CRAN.R-project.org/package=HDInterval
Monteiro LR, Furness RW (1998) Speciation through temporal segregation of Madeiran storm petrel (Oceanodroma castro) populations in the Azores? Philos Trans R Soc Lond B Biol Sci 353:945–953. https://doi.org/10.1098/rstb.1998.0259
Morris RD, Chardine JW (1995) Brown noddies on Cayo Noroeste, Culebra, Puerto Rico: what happened in 1990? Auk 112:326–334. https://doi.org/10.2307/4088720)
Morris-Pocock JA, Steeves TE, Estela FA, Anderson DJ, Friesen VL (2010) Comparative phylogeography of brown (Sula leucogaster) and red-footed boobies (S. sula): the influence of physical barriers and habitat preference on gene flow in pelagic seabirds. Mol Phylogenet Evol 54:883–896. https://doi.org/10.1016/j.ympev.2009.11.013
Murphy RC (1936) Oceanic birds of South America: a study of species of the related coasts and seas, including the American quadrant of Antarctica, based upon the Brewster-Sanford collection in the American Museum of Natural History. MacMillan Company, New York
Mussmann SM, Douglas MR, Chafin TK, Douglas ME (2019) BA3-SNPs: contemporary migration reconfigured in BayesAss for next-generation sequence data. Methods Ecol Evol 10:1808–1813. https://doi.org/10.1111/2041-210X.13252
Nabholz B, Lanfear R, Fuchs J (2016) Body mass-corrected molecular rate for bird mitochondrial DNA. Mol Ecol 25:4438–4449. https://doi.org/10.1111/mec.13780
Nunes GT, Bugoni L (2017) Local adaptation drives population isolation in a tropical seabird. J Biogeogr 45:332–341. https://doi.org/10.1111/jbi.13142
Nunes GT, Mancini PL, Bugoni L (2017) When Bergmann’s rule fails: evidences of environmental selection pressures shaping phenotypic diversification in a widespread seabird. Ecography 40:365–375. https://doi.org/10.1111/ecog.02209
Nuss A, Carlos CJ, Moreno IB, Fagundes NJ (2016) Population genetic structure of the magnificent Frigatebird Fregata magnificens (Aves, Suliformes) breeding colonies in the western Atlantic Ocean. PLoS ONE 11:e0149834. https://doi.org/10.1371/journal.pone.0149834
Obiol JF, James HF, Chesser RT, Bretagnolle V, González-Solís J, Rozas J, Riutort M, Welch AJ (2021) Integrating sequence capture and restriction site-associated DNA sequencing to resolve recent radiations of pelagic seabirds. Syst Biol 70:976–996. https://doi.org/10.1093/sysbio/syaa101
Oksanen J, Blanchet FG, Friendly M, Kind R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2020) vegan: Community Ecology Package. R package version 2.5-7. See https://cran.r-project.org/web/packages/vegan/index.html
Orsini L, Mergeay J, Vanoverbeke J, De Meester L (2012) The role of selection in driving landscape genomic structure of the waterflea Daphnia magna. Mol Ecol 22:583–601. https://doi.org/10.1111/mec.12117
Oswald JA, Harvey MG, Remsen RC, Foxworth DU, Cardiff SW, Dittmann DL, Megna LC, Carling MD, Brumfield RT (2016) Willet be one species or two? A genomic view of the evolutionary history of Tringa semipalmata. Auk 133:593–614. https://doi.org/10.1642/AUK-15-232.1
Paradis E (2010) Pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics 26:419–420. https://doi.org/10.1093/bioinformatics/btp696
Paradis E, Schliep K (2019) Ape 5.0: an environment for modern phylogenetics and evolutionary analyses. R Bioinf 35:526–528. https://doi.org/10.1093/bioinformatics/bty633
Peck DR, Congdon BC (2004) Reconciling historical processes and population structure in the sooty tern Sterna fuscata. J Avian Biol 35:327–335. https://doi.org/10.1111/j.0908-8857.2004.03303.x
Perez-Correa J, Carr P, Meeuwig JJ, Koldewey HJ, Letessier TB (2020) Climate oscillation and the invasion of alien species influence the oceanic distribution of seabirds. Ecol Evol 10:9339–9357. https://doi.org/10.1002/ece3.6621
Pigliucci M (2005) Evolution of phenotypic plasticity: where are we going now? Trends Ecol Evol 20:481–486. https://doi.org/10.1016/j.tree.2005.06.001
Poplin R, Ruano-Rubio V, DePristo MA, Fennell TJ, Carneiro MO, Van der Auwera GA, Kling DE, Gauthier LD, Levy-Moonshine A, Roazen D, Shakir K, Thibault J, Chandran S, Whelan C, Lek M, Gabriel S, Daly MJ, Neale B, MacArthur DG, Banks E (2017) Scaling accurate genetic variant discovery to tens of thousands of samples. bioRxiv. https://doi.org/10.1101/201178
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959. https://doi.org/10.1093/genetics/155.2.945
Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Posterior summarisation in bayesian phylogenetics using Tracer 1.7. Syst Biol 67:901–904. https://doi.org/10.1093/sysbio/syy032
Rayner MJ, Hauber ME, Steeves TE, Lawrance HA, Thompson DR, Sagar PM, Bury SJ, Landers TJ, Phillips RA, Ranjard L, Shaffer SA (2011) Contemporary and historical separation of transequatorial migration between genetically distinct seabird populations. Nat Commun 2:332. https://doi.org/10.1038/ncomms1330
Rexer-Huber K, Veale AJ, Catry P, Cherel Y, Dutoit L, Foster Y, McEwan JC, Parker GC, Phillips RA, Ryan PG, Stanworth AJ, van Stijn T, Thompson DR, Water J, Robertson BC (2019) Genomics detects population structure within and between ocean basins in a circumpolar seabird: the white-chinned petrel. Mol Ecol 28:4552–4572. https://doi.org/10.1111/mec.15248
Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sánchez-Gracia A (2017) DnaSP 6: DNA sequence polymorphism analysis of large datasets. Mol Biol Evol 34:3299–3302. https://doi.org/10.1093/molbev/msx248
RStudio Team (2023) PBC, Boston, MA URL http://www.rstudio.com/
Schulz-Neto A (2004) Aves marinhas do Atol das Rocas. Aves Marinhas e Insulares Brasileiras: Bioecologia e Conservação (eds Branco, JO), pp 169–192. Itajaí: Editora da Univali
Stecher G, Tamura K, Kumar S (2020) Molecular Evolutionary Genetics Analysis (MEGA) for macOS. Mol Biol Evol 37:1237–1239. https://doi.org/10.1093/molbev/msz312
Surman CA, Wooller RD (2003) Comparative foraging ecology of five sympatric terns at a sub-tropical island in the eastern. Indian Ocean. J Zool, Long 259:219–230. https://doi.org/10.1017/S0952836902003047
Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595. https://doi.org/10.1093/genetics/123.3.585
Tange O (2018) GNU parallel 2018. https://doi.org/10.5281/zenodo.1146014
Taylor RS, Bolton M, Beard A, Birt T, Deane-Coe P, Raine AF, González-Solís J, Lougheed SC, Friesen VL (2019) Cryptic species and independent origins of allochronic populations within a seabird species complex (Hydrobates spp.). Mol Phyl Evol 139:106552. https://doi.org/10.1016/j.ympev.2019.106552
Van der Auwera GA, O’Connor BD (2020) Genomics in the Cloud: Using Docker, GATK, and WDL in Terra (1st Edition). California: O’Reilly Media
von Takach B, Ranjard L, Burridge CP, Cameron SF, Cremona T, Eldridge MDB, Fisher DO, Frankenberg S, Hill BM, Hohnen R, Jolly CJ, Kelly E, MacDonald AJ, Moussalli A, Ottewell K, Phillips BL, Radford IJ, Spencer PBS, Trewella GJ, Umbrello LS, Banks SC (2022) Population genomics of a predatory mammal reveals patterns of decline and impacts of exposure to toxic toads. Mol Ecol 31:5468–5486. https://doi.org/10.1111/mec.16680
Wang IJ, Bradburd GS (2014) Isolation by environment. Mol Ecol 23:5649–5662. https://doi.org/10.1111/mec.12938
Weir BS, Cockerham CC (1984) Estimating F-Statistics for the Analysis of Population Structure. Evol 38:1358–1370. https://doi.org/10.2307/2408641
Waples RS, Do C (2010) Linkage disequilibrium estimates of contemporary Ne using highly variable genetic markers: a largely untapped resource for applied conservation and evolution. Evol Appl 3:244–252. https://doi.org/10.1111/j.1752-4571.2009.00104.x
West-Eberhard MJ (1989) Phenotypic plasticity and the origins of diversity. Annu Rev Ecol Syst 20:249–278 https://doi.org/10.1146/annurev.es.20.110189.001341
Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177–1191. https://doi.org/10.1093/genetics/163.3.1177
Wilson JW, Wanless RM, Burle MH, Angel A, Kritzinger P (2010) Breeding biology of brown noddies Anous stolidus at their southern-most breeding site, Gough Island, in comparison to other sites. Ardea 98:242–246. https://doi.org/10.5253/078.098.0215
Winker K, Glenn TC, Faircloth BC (2018) Ultraconserved elements (UCEs) illuminate the population genomics of a recent, high-latitude avian speciation event. PeerJ 6:e5735. https://doi.org/10.7717/peerj.5735
Wright S (1943) Isolation by distance. Genetics 28:114–138. https://doi.org/10.1093/genetics/28.2.114
Zarza E, Faircloth BC, Tsai WL, Bryson RW Jr, Klicka J, McCormack JE (2016) Hidden histories of gene flow in highland birds revealed with genomic markers. Mol Ecol 25:5144–5157. https://doi.org/10.1111/mec.13813
Zink RM, Barrowclough GF (2008) Mitochondrial DNA under siege in avian phylogeography. Mol Ecol 17:2107–2121. https://doi.org/10.1111/j.1365-294X.2008.03737.x
Acknowledgements
We thank Patrícia Mancini for samples collected during her PhD which were used for genetic analysis in the current study; Gregory Thom e Silva, Vera de Ferran and Fábio Raposo do Amaral for their valuable assistance with bioinformatic analyses; Sandro Bonatto, Gregory Thom e Silva and Silvina Botta for their contributions to the final version of this manuscript; Bruno Andrade de Linhares for samples collected at Martin Vaz; Paul Gerhard Kinas for their helpful insights with Bayesian statistics; Gabriel Canani for help with figure editing. We are also thankful to Laboratório de Genética at FURG for sharing space and equipment where PCRs and sample preparation were carried out. We thank CEMAVE for the provided rings; the conservation units’ teams which cooperated with sampling; Marinha do Brasil, Programa de Pesquisas Científicas da Ilha da Trindade (PROTRINDADE) and Programa Arquipélago de São Pedro e São Paulo (PROARQUIPELAGO). We are also thankful for the valuable suggestions provided by the two anonymous reviewers.
Funding
MSM and VM were supported by Master’s fellowships from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq). LB is a research fellow of CNPq (310145/2022-8) and NJRF is funded by Fundação de Amparo à Pesquisa do Estado do RS (FAPERGS).
Author information
Authors and Affiliations
Contributions
Conceptualization: MSM, LB; Data curation: MSM, VM; Formal analysis: MSM, NJRF, VM; Funding acquisition: LB; Investigation: MSM, NJRF, VM, LB; Methodology: MSM, NJRF, VM; Project administration: MSM; Resources: LB; Software: MSM; Supervision: LB, NJRF; Validation: MSM; LB, NJRF; Visualization: MSM; Writing – original draft: MSM; Writing – review & editing: MSM; LB; NJRF, VM.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Ethical approval
For this work was provided by Animal Use Ethics Committee from Universidade Federal do Rio Grande (FURG) under the process number 23116.002603/2021-87 and report PRF037/2022. Sampling was conducted under the approval from Sistema de Autorização e Informação em Biodiversidade (license numbers 76,380 and 22,697).
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Mazzochi, M.S., Muraro, V., Fagundes, N.J.R. et al. Absence of genetic structure among ecologically diverse populations indicate high plasticity in a pantropical seabird. Conserv Genet (2024). https://doi.org/10.1007/s10592-024-01613-x
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10592-024-01613-x